2004 EndodtopicsHaapasaloetal PDF
2004 EndodtopicsHaapasaloetal PDF
2004 EndodtopicsHaapasaloetal PDF
Apical periodontitis is an inflammatory process in the periradicular tissues caused by microorganisms in the necrotic
root canal. Accordingly, to achieve healing of apical periodontitis, the main goal of the treatment must be
elimination of the infection and prevention of re-infection. As shown by recent epidemiological studies in several
countries around the world, post-treatment endodontic disease is a far too common finding. To understand the
reasons for survival of resistant bacteria in the filled root canal, it is important to know in detail the interaction
between treatment procedures and the root canal flora in primary apical periodontitis. Therefore, in the first half of
this review, the focus is placed on control of infection in primary apical periodontitis. This is followed by a detailed
description of the resistant root canal microflora and a discussion about the present and future strategies to
eliminate even the most resistant microbes in post-treatment disease.
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Intracanal infection
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Intracanal infection
Variation in bacterial penetration patterns within penetrating into the dentine, using strepavidin–biotin
different portions of root canals has been little studied. labeling. Fusobacterium nucleatum, Eubacterium alac-
In an in vitro study with Streptococcus gordonii, Love tolyticum, E. nodatum, Lactobacillus casei, and Peptos-
(36) showed that in the coronal and middle portions of treptococcus micros were the most frequently detected
the root canals bacterial invasion into tubules was species. It is noteworthy that F. nucleatum is a Gram-
similarly effective and much greater than in the apical negative anaerobic rod, and all others were Gram-
portion of the canals. Obviously, in a clinical situation positive anaerobic rods and cocci (34).
in vivo, composition of the flora, patency of the Although the dominance of Gram-positive bacteria in
dentinal tubules, and availability of nutrients, in dentine samples seems quite convincing, there are
particular, may play a major role in regulating or reports also showing a strong invasion of dentinal
stimulating bacterial invasion of the dentine in various tubules by Gram-negative anaerobic bacteria (34).
parts of the root canal. Both in vitro studies (33, 37) Martin et al. (28) studied bacteria found in the carious
and in vivo observations (38) have clearly shown that dentine of 65 teeth extracted from patients with
removal of root surface cementum by mechanical advanced caries and pulpitis. Analysis of cultured
means or by surface resorption, such as typically bacteria showed a predominance of lactobacilli and
seen histologically in the apical area of teeth with other Gram-positive microorganisms. Gram-negative
apical periodontitis, greatly facilitates invasion of bacteria were also present in significant numbers, with
bacteria into dentinal tubules. Stanley et al. (39) Prevotella spp. being the most numerous anaerobic
reported that dentinal sclerosis in the root was not group cultured. With real-time PCR analysis of the
related to external stimuli such as caries, but rather powdered dentine, the relative proportion of Gram-
related to increasing age. Dentinal sclerosis extended negative anaerobes was somewhat higher than when
with age from the apical towards the cervical area. culturing was used. Prevotella spp., Fusobacterium spp.,
This could mean that among older people bacterial Porphyromonas gingivalis, and P. endodontalis were
invasion of dentinal tubules, in particular in the apical among the frequently detected species.
portions of canals, is less pronounced than in young Invasion into dentinal tubules by Gram-negative
patients. bacteria from periodontal pockets has been reported by
Ando & Hoshino (40) studied the composition of Giuliana et al. (41). Microorganisms identified in-
the microflora invading the deep layers of root canal cluded putative periodontal pathogens such as Pre-
dentin (0.5–2.0 mm from the surface of the root canal votella intermedia, Porphyromonas gingivalis, F.
wall) of human root canals by sampling the split nucleatum, and Bacteroides forsythus (present name
surfaces of eight freshly extracted teeth in an anaerobic Tannerella forsythensis), all frequently found in primary
chamber. More bacteria were recovered after anaerobic apical periodontitis.
incubation than after aerobic incubation in air with 30% The mechanisms by which the bacteria invade
CO2. Out of 256 predominant bacteria isolated, 80% dentinal tubules are not fully understood. However,
were obligately anaerobic species. Lactobacillus spp. the ability to penetrate dentinal tubules does not seem
(30%) and Streptococcus spp. (13%) were predominant, to be dependent on the motility of the bacterial cells. In
followed by Propionibacterium sp. (9%). In this study, fact, most of the species that best invade the tubules are
obligately anaerobic Gram-negative rods were not nonmotile. Love et al. (42) found that the streptococ-
found. The authors concluded that the microflora cal antigen I/II family of polypeptides are involved in
found in the deep layers of infected root dentine the attachment of oral streptococci to collagen, and
resembled that of the deep layers of carious lesions in that they also determine the ability of these bacteria to
coronal dentine. Recently, Matsuo et al. (34) showed invade dentinal tubules of human teeth. It has also been
bacterial invasion into dentinal tubules in 70% of 40 shown that while serum prevented dentinal invasion by
teeth extracted for apical periodontitis. When the root S. mutans and S. gordonii, the invasion by E. faecalis
canals were instrumented, the frequency of bacteria was only reduced but not totally prevented (43).
found in the dentinal tubules was almost as high, with Salivary molecules mucin and immunoglobulin G
65% of the teeth still showing dentinal invasion by (IgG), which co-aggregate with bacterial cells, also
bacteria. Antibodies against 16 selected oral bacteria inhibit dentine invasion (43). In addition, the deposi-
were used in the same study to identify the species tion of dentinal tubule fluid molecules e.g. albumin,
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Intracanal infection
Fig. 5. (A) Apical periodontitis in two lower incisor teeth. (B) Four months control after the canals were filled with
calcium hydroxide. (C) Six months control. Continued healing can be seen (D). The teeth were root filled at 6 months.
(E) One-year control radiograph shows complete healing of apical periodontitis lesions.
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Intracanal infection
bacterial elimination and facilitates removal of necrotic been increasing. Although studies comparing the
tissue and dentine chips from the root canal; thus antibacterial effect of NaOCl and CHX have produced
irrigants prevent packing of infected tissue apically in somewhat conflicting results, it seems that when used
the root canal and into the periapical area. In addition, in identical concentrations, their antibacterial effect in
many irrigating solutions have other beneficial effects. the root canal and in infected dentine is similar (29, 58–
EDTA (ethylene–diammine–tetra-acetic acid, 17% 60). However, CHX lacks the tissue-dissolving ability,
disodium salt, pH 7) is a chelating agent widely used which is one of the obvious benefits of NaOCl.
in endodontic preparation. It has low or no antibacter- Waltimo et al. (61) studied the antifungal effect of
ial activity, but it effectively removes smear layer by combinations of endodontic irrigants and found that
affecting the inorganic component of the dentine. the combinations of disinfectants were equally or less
Therefore, by facilitating cleaning and removal of effective than the more effective component when used
infected tissue, EDTA contributes to the elimination alone. However, it has been shown that in certain
of bacteria in the root canal. It has also been shown that concentrations chlorhexidine and hydrogen peroxide
removal of the smear layer by EDTA (or citric acid) have a strong synergistic effect against Enterococcus
improves the antibacterial effect of locally used disin- faecalis, Streptococcus sobrinus, and Staphylococcus aur-
fecting agents in deeper layers of dentine (29, 52). eus (58, 62).
Sodium hypochlorite (NaOCl), used in concentra-
tions varying from 0.5% to 5.25%, is a strong
Rotary instrumentation
antimicrobial agent, which plays an important role in
dissolving the organic part of pulpal remnants and The use of rotary preparation with nickel–titanium
dentine. Most importantly, it kills bacteria very rapidly (NiTi) instruments undoubtedly offers several poten-
even at relatively low concentrations. Pashley et al. (53) tial advantages. The most obvious of these are probably
demonstrated greater cytotoxicity and caustic effects the quality of the apical preparation and efficiency.
on healthy tissue with 5.25% NaOCl than with 0.5% However, rotary instruments have not always com-
and 1% solutions. No in vivo studies have clearly shown pared favorably when the various aspects of preparation
that the stronger solutions have a better antibacterial have been analyzed (63). Ahlquist et al. (64) showed
effect in the root canal. However, careless use of both that hand instrumentation produced cleaner canals
NaOCl (in high and low concentrations) as well as than preparation with rotary instruments. Similar
EDTA will result in severe pain and extensive tissue results have been reported by Schafer & Lohmann
damage if they are introduced to the periapical area (65). Nevertheless, rotary NiTi instruments appear to
(54). Niu et al. (55) observed the ultrastructure on maintain the original canal curvature better than hand
canal walls after EDTA and combined EDTA plus stainless-steel instruments, particularly in the apical
NaOCl irrigation by scanning electron microscopy. part of the root canal (66).
They reported that more debris was removed by Dalton et al. (67) compared stainless-steel K-type
irrigation with EDTA followed by NaOCl than with files and NiTi rotary instruments in removing bacteria
EDTA alone. Byström & Sundqvist (56, 57) showed from infected root canals with saline as an irrigant. Only
that although 0.5% NaOCl, with or without EDTA, approximately one-third of the canals were rendered
improved the antibacterial efficiency of preparation, all bacteria-free, and no significant difference could be
canals could not be rendered bacteria-free even after detected between the two groups. However, larger
repeated appointments. preparation diameter of the apical canal produced a
NaOCl effectively kills bacteria, but is caustic if significant reduction in bacterial counts. Coldero et al.
accidentally expressed into the periapical area. In (68) studied the effect of apical preparation on the
addition, the active chlorine in the solution may number of residual bacteria in the root canal. They
damage patients’ clothing through its strong bleaching concluded that additional apical enlargement to size
effect. Therefore, alternative irrigating solutions have #35 did not further reduce the number of surviving
been pursued that could replace NaOCl. Chlorhexidine bacteria. However, the size of the original preparation
gluconate (CHX) has been in use for a long time in was not given, and it is possible that the size #35 was
dentistry because of its antimicrobial properties and its too small to show differences in bacterial elimination.
relatively low toxicity, and its use in endodontics has In fact, Rollison et al. (69) showed that apical
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Haapasalo et al
enlargement to size #50 instead of size #35 resulted in a canals offers one explanation as to why in the clinical
more effective elimination of bacteria in the root canal, study (70) it was difficult to eliminate bacteria from
although sterility was not obtained. such canals totally as compared with canines and
In a recent study, Card et al. (70) reported sterility in premolars.
a majority of root canals instrumented by rotary NiTi
instruments using large apical sizes and irrigation with
Size of the apical preparation
1% NaOCl. The instrumentation and bacterial sam-
pling were carried out in two phases: the first The main goals of mechanical preparation are as
instrumentation utilized 1% NaOCl and 0.04 taper follows: (i) to remove infected tissue from the root
ProFile rotary files. The cuspid and bicuspid canals were canal, (ii) to facilitate the use and effectiveness of
instrumented to size #8 and the molar canals to size #7. irrigating solutions, (iii) to create sufficient space for
The second instrumentation utilized LightSpeed files effective delivery of intracanal medicaments between
and 1% NaOCl irrigation for further enlargement of the appointments, and (iv) to create sufficient space in the
apical third. Typically, canals of molars were instru- root canal to allow placement of permanent root filling
mented to size #60 and cuspid/bicuspid canals to size of high quality. Despite these clearly defined and widely
#80. All of the cuspid/bicuspid canals and 81.5% of the accepted general goals for preparation, there is no
molar canals were bacteria-free already after the first consensus about the recommended size for the apical
instrumentation, as shown by negative cultures from preparation in various teeth. Theoretically, optimal
samples obtained from the root canals. In the molars, apical preparation would require an instrument size
bacteria-free canals increased to 89% after the second equal to or bigger than the largest diameter of the apical
instrumentation. When the molar canals were divided canal. This would guarantee that all walls in this
into two groups, one with no visible anastomoses critically important part of the canal would be engaged
between root canals and the other with a complex root by the instruments. Studies by Kerekes & Tronstad
canal anatomy, the proportion of sterile canals in the (72–74) suggested that the final preparation size
first group was 93% already after the first instrumenta- should be quite large as compared with the sizes often
tion. The results of Card et al. (70) are indirectly used in practice: size #50 to #90 in incisors, canines and
supported by earlier observations by Peters et al. (71), premolars, and even in molar curved canals sizes #50 to
who studied rotary preparation of root canals of #60. These studies also demonstrated that in oval-
maxillary first molars. They compared the effects of shaped roots, such as in maxillary first premolars, it was
four preparation techniques on canal volume and often impossible to obtain a round apical preparation
surface area using three-dimensionally reconstructed without perforation of the root, because the narrow
root canals in extracted teeth. Micro CT data were used external dimension of the root in several teeth was
to describe morphometric parameters related to the smaller than the larger internal diameter of the root
four preparation techniques. Specimens were scanned canal. The same was concluded in another study of
before and after canals were prepared using K-type maxillary first molars by Gani & Visvisian (75).
hand files, LightSpeed instruments, ProFile .04 and GT In clinical practice, there are no available methods
rotary instruments. Differences in dentine volume that would reliably gauge the size of the apical root
removed, canal straightening, the proportion of unin- canal. Morfis et al. (76) studied the size of apical
strumented area, and canal transportation were calcu- foramina in various tooth groups and found that the
lated (71). The results showed that instrumentation of largest foramen was in the distal root of lower molars,
canals increased their volume and surface area. The the average diameter being almost 0.4 mm (size #40).
prepared canals were significantly more rounded, had Wu et al. (77) studied if the first file to bind apically
greater diameters, and were straighter than unprepared would correspond to the diameter of the canal in the
canals. However, all instrumentation techniques left at apical region. The canals were prepared three sizes
least 35% of the canals’ surface area untouched. There larger than the first binding file, and the quality of the
were significant differences between the three canal final preparation was then analyzed. The result of this
types investigated; however, very few differences were study showed that there was no correlation between the
found between instrument types. The relatively large first binding file and the larger diameter of the apical
proportion of untouched canal walls in molar root canal. At present, the typical size of the apical
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agents than other endodontic microbes (52). In vitro calcium hydroxide may help to better remove the
and in vivo studies have clearly demonstrated that residual necrotic pulp tissue at the second appointment,
intracanal calcium hydroxide fails to eliminate E. as well as neutralize bacterial antigens remaining in the
faecalis from the infected dentine (52, 91). On the root canal system (98, 99).
other hand, no other medicament has shown better in
vivo effectiveness against E. faecalis either (91).
Root filling and permanent restoration
However, although there is a good agreement about
the dominance of E. faecalis in retreatment cases of Eventually, all locally used disinfectants lose their
apical periodontitis, the importance of this bacterium antibacterial effect over time or are washed away from
for the long-term prognosis of the retreatment has not the canal through the apical foramen. Permanent root
been demonstrated in clinical studies. Other microbes filling is therefore necessary to prevent bacteria from re-
frequently found in retreatment cases include Gram- entering the root canal space after chemomechanical
positive facultative organisms such as Streptococcus spp., preparation and disinfection. It has also been suggested
Lactobacillus spp., Actinomyces spp., Propionibacterium that the root filling may entomb the residual bacteria in
spp., Gram-negative coliform rods, and the yeast the root canal system so that they cannot proliferate and
Candida albicans (15, 92, 93). interact with the periapical tissue, which could com-
Root canal disinfecting agents are extremely effective promise healing. However, there are very little data
against even the resistant microbes when tested in a available about the effectiveness of such root canal
test-tube environment. The clearly poorer results in bacteria entombment by the root filling. Sjögren et al.
vivo in the root canal indicate the presence of (6) demonstrated the importance of obtaining negative
interfering factors that negatively affect the outcome cultures for improving the prognosis of the treatment
of the disinfection. Haapasalo et al. (94) and Portenier of apical periodontitis. However, Peters & Wesselink
et al. (95, 96) studied the effect of dentine and other (8) found no difference in healing of teeth with apical
substances present in the root canal milieu on the periodontitis filled after negative or positive culture at
antibacterial effect of commonly used intracanal the time of filling. The latter would mean that more
medicaments, such as calcium hydroxide, chlorhexi- bacteria were ‘entombed’ by the root filling. Katebza-
dine, and IPI against E. faecalis. These studies showed deh et al. (7, 100) simulated such entombment in dog
that all three disinfectants were negatively affected by teeth that were experimentally infected and developed
the various substances tested, calcium hydroxide being apical lesions. Some of the canals were obturated at the
particularly sensitive to the inhibitory effect of a variety first appointment after instrumentation and irrigation
of substances present in the root canal. Earlier, Messer with saline, while the rest were disinfected before root
& Chen (97) had reported on the short duration of the canal filling with an interappointment calcium hydro-
vapors from cotton pellets soaked in phenol com- xide dressing. The results showed better healing in
pounds. The inactivation of locally used disinfecting teeth where calcium hydroxide had been used. How-
agents in the root canal may explain the relative ever, the apical anatomy of dog teeth is quite different
resistance of the root canal microflora. Gram-positive from that of human teeth, which may have affected the
facultative bacteria, which best tolerate the harsh results. Hernandez et al. (101) evaluated the root canal
ecological conditions created by the chemomechanical morphology in 72 maxillary fourth premolars and 59
preparation, have been shown to increase their relative mandibular first molars in dogs. An apical delta was
proportion of the flora after preparation and use of present in all roots (n 5 334) and represented approxi-
disinfection, even though the total numbers are mately 12–18% of the total root length for all roots.
strongly reduced by the treatment procedures (15, 92). In a new study using infected dentine blocks in vitro,
At present, it seems correct to conclude that no Saleh et al. (102) showed that root filling with gutta-
interappointment root canal disinfectant can predicta- percha and specific sealers (AH plus or Grossman’s
bly render canals sterile in the treatment of teeth with sealer) was clearly more effective in eliminating E.
apical periodontitis. However, it is clear from most faecalis from the dentine surrounding the root canal
studies that the use of the intracanal medicaments than calcium hydroxide 1 week after filling. Root
further reduces the number of infecting microorgan- fillings with gutta-percha and several other sealers
isms after chemomechanical preparation. Furthermore, proved to be less effective than calcium hydroxide
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Intracanal infection
against E. faecalis dentine infection (102). The result home in Finland. Only 16% of the 507 root-filled teeth
supported an earlier observation by Ørstavik (103) that had apical periodontitis.
AH 26 was clearly more effective in killing bacteria in It should be emphasized that the great majority of
dentine around the root canal than other sealers tested. root-filled teeth with apical periodontitis (post-treat-
It may be of interest that in the study of Peters & ment disease) are symptom-free, and no clinical,
Wesselink (8), AH 26 was used as the sealer. Clearly, in histological, or bacteriological investigation has been
future studies comparing the outcome of single- included in most of the epidemiological studies.
appointment and two-appointment endodontic treat- Although some of these teeth may have been treated
ment of apical periodontitis, the type of the sealer also only recently, and thus may reflect healing in progress,
has to be taken into consideration. it is likely that most of these lesions will not heal
Finally, all root fillings must be protected by a coronal without some kind of intervention. It is possible that (i)
restoration of high quality. Lack of coronal restoration the original apical periodontitis lesion has not healed
or leaking restorations may result in bacterial contam- after the primary endodontic therapy, (ii) the lesion has
ination of the whole root filling in as little as a couple of persisted after retreatment, (iii) the original lesion has
weeks (104). Although the clinical relevance of coronal healed but a new lesion has later emerged, and (iv)
leakage has not yet been convincingly demonstrated, it there was no lesion at the time of endodontic
is obvious that coronal leakage plays an important role treatment, but a lesion has developed over time. There
in the etiology of post-treatment disease. is no reliable information available about the propor-
tion of each group, but clinical experience and follow-
up studies have shown that they all occur. Therefore, it
Post-treatment disease (persistent may be misleading to call categorically all root-filled
teeth with a lesion as ‘endodontic failures’. In fact,
endodontic infection)
endodontic treatment may have resulted in healing, but
Epidemiological studies of root-filled teeth in various subsequent coronal leakage, for example as a conse-
countries and different populations have demonstrated quence of caries, may have caused the recurrence of
the presence of apical periodontitis in a relatively high disease.
proportion of these teeth (105–112). In a large study of
the quality of endodontic treatment in a Belgian
Microbial flora of primary apical
population, De Moor et al. (105) evaluated the
periodontitis
periapical conditions in 4617 teeth of 206 adults using
panoramic radiographs. Of all the teeth, 6.8% were As stated earlier in this review, the ecological conditions
endodontically treated. Comparison of periapical status in the necrotic root canal are the main selective factors
showed that apical periodontitis was found in 6.6% of for the microbial flora in primary apical periodontitis.
all teeth, and in 40.4% of all root-filled teeth. Therefore, the flora is characterized by a strong
Inadequate level of the root canal filling was registered dominance of obligately anaerobic bacteria (Fig. 13)
in over 50% of these teeth. In another study in (25, 26, 115–131). The most frequent isolates are
Denmark (111), the periapical status of nearly 600 Dialister pneumosintes (Bacteroides pneumosintes), T.
root-filled teeth was compared in 1974–1975 and forsythensis (B. forsythus), Prevotella spp., Porphyromo-
1997–1998. Apical periodontitis was observed in nas spp., Fusobacterium spp., Treponema spp., Campy-
approximately 50% of the root-filled teeth in both lobacter rectus (Wolinella recta), Micromonas micros (P.
groups, and in molars the prevalence of disease was as micros), Eubacterium spp., Bifidobacterium spp., Acti-
high as 65% in both groups. In a Lithuanian popula- nomyces spp., Propionibacterium spp., Lactobacillus
tion, the frequency of apical periodontitis in root-filled spp., and Streptococcus spp. Most of the above genera
teeth was 35% (110), while in two selected Canadian are obligately anaerobic; Actinomyces, Propionibacter-
populations, the prevalence of apical periodontitis in ium and Lactobacillus contain both anaerobic and
root-filled teeth was 44% and 51% (113). The lowest facultatively anaerobic species and strains, while strep-
prevalence of apical periodontitis in root-filled teeth tococci are facultative bacteria. E. faecalis is usually not
was reported by Soikkonen (114), who studied 133 found in primary apical periodontitis. However, using
dentate old people aged 76, 81, and 86 years living at checkerboard DNA–DNA hybridization, Siqueira et al.
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Haapasalo et al
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Intracanal infection
treatment procedures and to the various materials used treatment, but it is more likely to be the consequence of
during the treatment and in the root fillings. Ecological coronal leakage.
changes also play a major role in selecting species that
best resist the antibacterial effect of the chemicals and
Microflora in root-filled teeth with apical
try to adapt to the new ecological milieu. The
periodontitis
conclusion based on several studies is that facultative
species are more resistant than strictly anaerobic Research in endodontic microbiology has clearly been
bacteria, and Gram-positive bacteria are stronger characterized by a greater interest in primary apical
survivors than Gram-negative bacteria (13–16, 25, periodontitis than in post-treatment apical period-
26, 115–132). In root-filled teeth, the space available ontitis. However, interest in the microbiological profile
for microbes is limited as compared with the necrotic of post-treatment apical periodontitis has increased
root canals in primary apical periodontitis. Conse- considerably during the last few years. This may be
quently, the cfu counts obtained from retreated teeth mainly because of the perceived poorer prognosis of
are lower on average than those obtained from teeth retreatment as compared with primary treatment of
with primary apical periodontitis. Peciuliene et al. (15) infected root canals (89, 134). It has been suggested
reported a range between 40 and 7 107 cfu in that the differences in the outcome of treatment may be
microbiological samples obtained from 40 previously related to marked differences in the composition of the
root-filled teeth with asymptomatic apical period- microbial flora in the necrotic root canals (13). In post-
ontitis. The number of species and strains per canal is treatment apical periodontitis anaerobic bacteria con-
also clearly lower than in teeth with primary apical stitute the minority, and they are isolated less fre-
periodontitis. Typically one to three different species quently. E. faecalis is the dominant species present in
are isolated per canal, the average being close to one post-treatment apical periodontitis. It is the most
strain, whereas in primary apical periodontitis three to frequently isolated species and is usually also the
10 different strains are usually found, with the average predominant isolate in the canal (13–16, 89, 135).
of six species (13–15, 25, 26). The highest frequencies of isolation of E. faecalis have
been reported by Peciuliene et al. (15) and Pinheiro et
al. (135), at 64% and 53% of the culture-positive teeth,
Microflora in root-filled teeth without apical
respectively. The corresponding frequency in a North
periodontitis
American population reported by Hancock et al. (16)
In an infected, necrotic root canal, the presence of was 30%.
bacteria is invariably associated with the presence of Other bacteria frequently found in root-filled teeth
apical periodontitis (4, 26). However, when the root with apical periodontitis are alpha- and non-hemolytic
canal space is filled with a root-filling material, bacterial streptococci, Actinomyces spp., Lactobacillus spp., and
presence in the canal is not always accompanied by the Propionibacterium spp., all facultative or microaero-
presence of disease. Molander et al. (13) sampled root philic species (some Actinomyces and Lactobacillus
canals of 20 root-filled teeth that did not have apical strains and species are obligate anaerobes). Staphylo-
periodontitis. Thirteen microbial strains were found in coccus spp. are also found more frequently than in
nine of the 20 teeth. The microbes included one strain primary apical periodontitis (13, 16, 89, 135, 136).
of E. faecalis, streptococci and Gram-positive faculta- Gram-negative enteric rods and other facultative
tive rods, one strain of F. nucleatum (Gram-negative Gram-negative rods have also been reported from root
anaerobic rod), and two strains of the yeast C. albicans. canal samples of teeth with post-treatment apical
The cfu counts per canal were lower than in root-filled periodontitis. The species isolated include Enterobacter
teeth associated with apical periodontitis included in cloacae, E. agglomerans, Escherichia coli, Klebsiella
the same study. The absence of infection and disease in pneumoniae, Klebsiella oxytoca, Klebsiella sp., Citro-
root-filled teeth that harbor bacteria in the root canal bacter freundii, Acinetobacter sp., Pseudomonas aeru-
space can be explained by the lack of communication ginosa, Pseudomonas sp., Proteus mirabilis, and Proteus
between the bacteria in the root canal and the host sp. (13, 15, 88, 136).
tissues. The microbial flora in such teeth may be a Anaerobic bacteria are clearly in minority, and their
residual flora from an earlier infection that survived the frequency of isolation in root-filled teeth is below 50%
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Haapasalo et al
46
Intracanal infection
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48
Intracanal infection
both and sealed with an IRM top filling, whereas that of GE. Using a similar methodology, Tronstad et
control teeth were left unsealed. IRM considerably al. (156) evaluated the periapical status in 1001 teeth.
delayed but did not prevent bacterial penetration Full-mouth series of radiographs from randomly
through the root canal. No statistically significant selected patient charts at the Dental Faculty, University
differences were detected between the medicament of Oslo (Norway) were examined. The two groups with
groups (152). technically GEs had the least occurrence of disease. API
A potential limitation in the majority of studies on for the combined GE1GR was 81%, compared with
coronal bacterial leakage is their inability to quantify 71% for GE1PR. Groups with technically PEs had
leakage. However, Barrieshi et al. (153) assessed significantly lower API rates, regardless of the quality of
bacterial leakage of a mixed anaerobic community of coronal restoration (PE1GR, 56% and PE1PR, 57%).
organisms by F. nucleatum, P. micros, and C. rectus in In a study by Kirkevang et al. (157), a total of 614
filled canals after post-space preparation. Colonization randomly selected individuals (20 to over 60 years of
of the apical canal space was observed by scanning age) from Aarhus County (Denmark) had a full-mouth
electron microscopy. Eighty percent of the teeth radiographic examination. The quality of endodontic
demonstrated coronal leakage of F. nucleatum and C. and coronal restorations and the periapical status of
rectus within 90 days, with bacterial penetration root-filled teeth were assessed by radiographic criteria.
occurring from 48 to 84 days. Scanning electron GR was associated with better periapical status than PR
microscope examination showed a heterogeneous (API 52.0% vs. 36.1%). When both root filling and
biofilm of various bacterial morphotypes at the apical coronal restoration quality were assessed, API rates
canal wall. ranged from 68.8% (combined optimal quality) to
21.7% (all parameters scored as inadequate). In a recent
study, both clinical and radiographic criteria were used
Clinical relevance of coronal leakage
to evaluate the periapical, endodontic, and coronal
As opposed to the great number of studies demonstrat- status of 745 root-filled teeth, randomly selected from
ing coronal leakage in vitro, very few studies have patients attending Ghent University Dental School
focused on its clinical relevance. Friedman et al. (154) (Belgium) (158). Interestingly, when only clinical
observed the degree of periradicular inflammation in scoring was used to evaluate the quality of coronal
root-filled dog teeth, 6 months after inoculating the restoration, API rates for GR and PR did not differ
coronally sealed pulp chamber with plaque, and significantly (68.9% and 63.2%). However, when
compared it with teeth where no inoculation was evaluation was based on radiographic examination,
performed. Severe inflammation was detected in API rates for GR and PR (76.2% and 50.9%) differed
histological sections in seven of 48 coronally inoculated significantly. The significance of the quality of coronal
teeth (15%) and in one of 23 non-inoculated teeth (4%) restoration to periapical health of root-filled teeth was
without plaque sealed in the pulp chamber. Ray & also documented in two other recent studies in Canada
Trope (155) correlated the quality of both the root and India (113, 159). In the former, the coronal
filling and the permanent coronal restoration in 1010 restoration had an impact on API in teeth with PE, but
teeth with the periapical status as assessed from not in teeth with GE, corroborating the previous
radiographs. Full-mouth radiographs from randomly findings by Tronstad et al. (156).
selected new patient charts at Temple University A different approach to the role of coronal bacterial
Dental School (Philadelphia, PA, USA) were examined. leakage in periapical health was used by Ricucci et al.
A stronger correlation was found between the presence (160) and Ricucci & Bergenholtz (161), who analyzed
of a periapical lesion and poor coronal restoration than histologically 39 roots in 32 extracted teeth, all of
poor quality of endodontic treatment. The combina- which had been lacking coronal restoration for a
tion of good restoration (GR) and good endodontic minimum of 3 months. In some specimens, the root
(GE) quality had the highest absence of periradicular filling had been exposed to the oral environment for
inflammation (API) at 91.4%. This was significantly several years. As assessed by radiography, apical perio-
higher than poor restoration (PR) combined with poor dontitis was associated with five roots only (12.8%).
endodontic (PE) quality, with an API rate of only Brown and Brenn staining of longitudinal sections of
18.1%. The impact of GR appeared to be greater than 29 root specimens demonstrated the presence of
49
Haapasalo et al
bacteria along the main canal wall as well as in the system. In periapical actinomycosis, the infective flora,
dentinal tubules in the coronal third in 28 specimens. mainly Actinomyces species, has managed to establish
In one specimen bacteria were seen in the apical third of itself in the periapical area. In some cases of post-
the root canal, but not in the middle or coronal thirds. treatment apical periodontitis, it is possible that
One of the nine root specimens where the coronal third periapical inflammation is caused by a foreign body
was destroyed during extraction showed bacteria in the reaction, or may be connected to the presence of a large
apical third. Although based on a relatively small accumulation of cholesterol crystals (11, 12). The
sample, these two studies demonstrated that despite relative proportion of etiological reasons other than
prolonged exposure to the oral environment and oral microbes, however, is low. In addition, in order to
bacteria for several months and even years, a large-scale verify the diagnosis of non-microbial etiology, histo-
bacterial penetration into the filled root canal occurred pathological examination would be required. There-
only in the coronal portion of the root, while in the fore, from a practical point of view, whenever apical
apical portion the histological methods used failed to periodontitis has been diagnosed to affect a previously
disclose bacteria in the great majority of the roots. root-filled tooth, the treatment should target elimina-
tion of microbes. Consequently, the decision on new
treatment (retreatment) relies on the correct diagnosis
Coronal leakage: future
of the periapical status of the tooth. According to the
The evidence indicating the importance of coronal seal Consensus report of the European Society of Endodontol-
for the long-term outcome of endodontic therapy is ogy on quality guidelines for endodontic treatment (80),
quite convincing. It is reasonable, therefore, to empha- healing of apical periodontitis can be observed for up to
size the role of adequate, permanent coronal seal as an 4 years after the treatment (5 years after surgery),
integral part of endodontic therapy. However, many of before taking a decision on further intervention. The
the important details of bacterial coronal leakage and its prerequisite for this is that the tooth is symptom-free,
implications for clinical outcomes are yet to be and that the apical periodontitis lesion does not
uncovered. One of the central questions not yet become enlarged in the control radiographs. With
answered is when to recommend retreatment of a regard to differential diagnosis, it is important to
root-filled tooth, where the root filling has been exposed identify the possibility of healing with scar tissue (163,
directly or through leakage to oral bacteria. Our present 164), such as that may occur if both the buccal and
understanding is based on epidemiological studies and palatal cortex have been destroyed. Such may be the
indirect observations and conclusions. Because of many case in teeth associated with large lesions or after
ethical and practical reasons, the study design addressing periapical surgery (165).
this research question remains a challenge. Recently, In summary, post-treatment apical periodontitis is an
animal models were introduced for testing the effects of indication for endodontic treatment, where elimination
leakage on periradicular healing (154, 162). Areas not of the infection is the key for healing. Retreatment of
yet thoroughly studied are the composition of the teeth without apical periodontitis, but with an identified
invading microflora in coronal leakage in vivo, the effect risk for disease development, such as an apparently
of replacing only the coronal seal, without retreatment, deficient root filling or coronal leakage, is a more
on the contaminating microflora, and several quantita- complicated issue. The canal space in many of these teeth
tive aspects of coronal leakage in relation to apical is obviously contaminated, however, not to the extent
pathosis. Nevertheless, every effort should be taken to that causes disease. In such situations, too little is known
ensure good coronal seal during and after every about the risk of developing infection and disease in the
endodontic treatment. future, if coronal restoration is completed without first
performing endodontic retreatment.
50
Intracanal infection
provides very good outcomes, and healing can be already be achieved with today’s techniques and
expected in the great majority of teeth. Recent materials, future developments in these areas will
literature indicates, though, that in many teeth a small hopefully further improve our possibilities to eliminate
number of viable bacteria reside in the root canal predictably intracanal infection and prevent reinfection,
system, particularly in the dentinal tubules, at the time and thus prevent or heal apical periodontitis.
of root filling. Although these and other studies suggest
that these residual bacteria seldom interfere with
healing, there is no doubt that theoretically, residual Acknowledgements
bacteria pose a potential threat to long-term outcomes.
The authors wish to thank Dr Shimon Friedman for
Therefore, in an optimal situation, complete elimina-
constructive criticism and suggestions for improvement
tion of the residual microflora remains the goal of
during the preparation of this paper.
endodontic treatment. There is presently considerable
research activity on new methods and materials used for
instrumentation, irrigation, disinfection, and filling of
the root canal space to achieve more predictably
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